An overview of maternal separation effects on behavioural outcomes in mice: evidence from a four-stage methodological systematic review

Tractenberg, Saulo G.; Levandowski, Mateus L.; de Azeredo, Lucas Araújo; Orso, Rodrigo; Roithmann, Laura G.; Hoffmann, Emerson S.; Brenhouse, Heather; Grassi-Oliveira, Rodrigo

doi:10.1016/j.neubiorev.2016.06.021

Cited by 267Stress Responses and CortisolNeuroendocrine regulation and behaviorChild Abuse and Trauma

An overview of maternal separation effects on behavioural outcomes in mice: evidence from a four-stage methodological systematic review

Tractenberg, Saulo G., Levandowski, Mateus L., de Azeredo, Lucas Araújo, Orso, Rodrigo, Roithmann, Laura G., Hoffmann, Emerson S., Brenhouse, Heather, Grassi-Oliveira, Rodrigo·2016·Neuroscience & Biobehavioral Reviews

DOI 10.1016/j.neubiorev.2016.06.021

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Abstract

Early life stress (ELS) developmental effects have been widely studied by preclinical researchers. Despite the growing body of evidence from ELS models, such as the maternal separation paradigm, the reported results have marked inconsistencies. The maternal separation model has several methodological pitfalls that could influence the reliability of its results. Here, we critically review 94 mice studies that addressed the effects of maternal separation on behavioural outcomes. We also discuss methodological issues related to the heterogeneity of separation protocols and the quality of reporting methods. Our findings indicate a lack of consistency in maternal separation effects: major studies of behavioural and biological phenotypes failed to find significant deleterious effects. Furthermore, we identified several specific variations in separation methodological procedures. These methodological variations could contribute to the inconsistency of maternal separation effects by producing different degrees of stress exposure in maternal separation-reared pups. These methodological problems, together with insufficient reporting, might lead to inaccurate and unreliable effect estimates in maternal separation studies.

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Early life stress is known to impair (non-stressful) learning and memory.
“ELS – using a variety of models (Krugers and Joëls, 2014; Tractenberg et al., 2016) – is known to impair (non-stressful) learning and memory.”
From Effects of Maternal Deprivation and Complex Housing on Rat Social Behavior in Adolescence and Adulthood (2018) · cites this paper as Tractenberg et al., 2016
A difficulty in characterizing the maternal separation literature is the wide variety of separation methods, control groups, and statistical methods used.
“One difficulty in characterizing the maternal separation literature is the wide variety of separation methods, control groups, and statistical methods that have been utilized (Lehmann and Feldon, 2000; Tractenberg et al., 2016).”
From The effects of early life stress on reward processing (2018) · cites this paper as Tractenberg et al., 2016

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Epigenetic modifications induced by early enrichment are associated with changes in timing of induction of BDNF expression
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Strain-specific cognitive deficits in adult mice exposed to early life stress.
Mehta, M., & Schmauss, C. (2011) · Behavioral Neuroscience · doi:10.1037/a0021952 · Cited by 84 · see citing works
Single episode of maternal deprivation and adult depressive profile in mice: interaction with cannabinoid exposure during adolescence
Macrı̀, S., & Giovanni Laviola, A. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.02.009 · Cited by 82 · see citing works
Behavioral and hormonal responses to separation in infant rhesus monkeys and mothers.
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Effects of Diurnal Variation in Plasma Corticosterone Levels on Adrenocortical Response to Stress.
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Evaluating sex as a biological variable in preclinical research: the devil in the details
Tannenbaum, C., Schwarz, J. M., Clayton, J. A., Vries, G. J. D., & Sullivan, C. (2016) · Biology of Sex Differences · doi:10.1186/s13293-016-0066-x · Cited by 76 · see citing works
EFFECTS OF MATERNAL FACTORS UPON GROWTH AND BEHAVIOR OF THE RAT1
Denenberg, V. H., Ottinger, D. R., & Stephens, M. W. (1962) · Child Development · doi:10.1111/j.1467-8624.1962.tb05988.x · Cited by 74 · see citing works
Maternal behavior and offspring resiliency to maternal separation in c57bl/6 mice
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Behavioral and hormonal responses to separation in infant rhesus monkeys and mothers.
Levine, S., Johnson, D. F., & Gonzalez, C. A. (1985) · Behavioral Neuroscience · doi:10.1037/0735-7044.99.3.399 · Cited by 72 · see citing works
Importance of early lighting conditions in maternal care by dam as well as anxiety and memory later in life of offspring
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Neonatal Stress or Morphine Treatment Alters Adult Mouse Conditioned Place Preference
Boasen, J., McPherson, R. J., Hays, S. L., Juul, S. E., & Gleason, C. A. (2008) · Neonatology · doi:10.1159/000165379 · Cited by 62 · see citing works
Chronic exposure to a novel odor increases pups' vocalizations, maternal care, and alters dopaminergic functioning in developing mice
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The effect of early maternal separation on brain derived neurotrophic factor and monoamine levels in adult heterozygous reeler mice
Ognibene, E., Adriani, W., Caprioli, A., Ghirardi, O., Ali, S. F., Aloe, L., & Giovanni Laviola, A. (2008) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2008.03.023 · Cited by 60 · see citing works
Modulation of early stress-induced neurobiological changes: a review of behavioural and pharmacological interventions in animal models
Harrison, E. L., & Baune, B. T. (2014) · Translational Psychiatry · doi:10.1038/tp.2014.31 · Cited by 59 · see citing works
Long maternal separation accelerates behavioural sensitization to ethanol in female, but not in male mice
Kawakami, S. E., Quadros, I. M., Takahashi, S., & Suchecki, D. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.06.023 · Cited by 57 · see citing works
The scope for improving the design of laboratory animal experiments
Festing, M. F. W. (1992) · Laboratory Animals. Journal of the Laboratory Animal Science Association · doi:10.1258/002367792780745788 · Cited by 57 · see citing works
Early maternal separation impacts cognitive flexibility at the age of first independence in mice
Thomas, A. W., Caporale, N., Wu, C., & Wilbrecht, L. (2015) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2015.09.005 · Cited by 57 · see citing works
Implications of temporal variation in maternal care for the prediction of neurobiological and behavioral outcomes in offspring.
Jensen Peña, C., & Champagne, F. A. (2013) · Behavioral Neuroscience · doi:10.1037/a0031219 · Cited by 54 · see citing works
Early Life Stress Differentially Modulates Distinct Forms of Brain Plasticity in Young and Adult Mice
Herpfer, I., Hezel, H., Reichardt, W., Clark, K., Geiger, J., Gross, C. M., Heyer, A., Neagu, V., Bhatia, H. S., Atas, H. C., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0046004 · Cited by 51 · see citing works
Early life stress effects on adult stress-induced corticosterone secretion and anxiety-like behavior in the C57BL/6 mouse are not as robust as initially thought
Parfitt, D. B., WALTON, J., Corriveau, E. A., & Helmreich, D. L. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.06.002 · Cited by 51 · see citing works
Circadian‐ and temperature‐specific effects of early deprivation on rat maternal care and pup development: Short‐term markers for long‐term effects?
Rüedi‐Bettschen, D., Feldon, J., & Pryce, C. R. (2004) · Developmental Psychobiology · doi:10.1002/dev.20014 · Cited by 46 · see citing works
Neonatal Maternal Separation Alters Immune, Endocrine, and Behavioral Responses to Acute Theiler’s Virus Infection in Adult Mice
Meagher, M. W., Sieve, A. N., Johnson, R. R., Satterlee, D. M., Belyavskyi, M., Mi, W., Prentice, T. W., Welsh, T. H., & Welsh, C. J. (2010) · Behavior Genetics · doi:10.1007/s10519-010-9333-5 · Cited by 45 · see citing works
Long-term effects of neonatal stress on adult conditioned place preference (CPP) and hippocampal neurogenesis
Hays, S. L., McPherson, R. J., Juul, S. E., Wallace, G. N., Schindler, A. G., Chavkin, C., & Gleason, C. A. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.10.033 · Cited by 42 · see citing works
Increased vulnerability to ethanol consumption in adolescent maternal separated mice
García‐Gutiérrez, M. S., Navarrete, F., Aracil-Fernández, A., Bartoll, A., Martínez‐Gras, I., Lanciego, J. L., Rubio, G., & Manzanares, J. (2015) · Addiction Biology · doi:10.1111/adb.12266 · Cited by 40 · see citing works
Early experiences: Building up the tools to face the challenges of adult life
Branchi, I., & Cirulli, F. (2014) · Developmental Psychobiology · doi:10.1002/dev.21235 · Cited by 40 · see citing works
Neuropeptides as mediators of the early-life impact on the brain; implications for alcohol use disorders
Nylander, I., & Roman, E. (2012) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2012.00077 · Cited by 40 · see citing works
Some effects of strain differences in the maternal behavior of inbred mice
Ward, R. M. (1980) · Developmental Psychobiology · doi:10.1002/dev.420130209 · Cited by 39 · see citing works
Surveying the literature from animal experiments: Systematic review and meta-analysis are important contributions
Macleod, M. R., Ebrahim, S. B. J., & Roberts, I. (2005) · BMJ · doi:10.1136/bmj.331.7508.110-b · Cited by 37 · see citing works
Effects of Maternal Factors upon Growth and Behavior of the Rat
Denenberg, V. H., Ottinger, D. R., & Stephens, M. W. (1962) · Child Development · doi:10.2307/1126633 · Cited by 36 · see citing works
Protective effects of intermittent hypoxia on brain and memory in a mouse model of apnea of prematurity
Bouslama, M., Adle‐Biassette, H., Ramanantsoa, N., Bourgeois, T., Bollen, B., Brissaud, O., Matrot, B., Gressèns, P., & Gallego, J. (2015) · Frontiers in Physiology · doi:10.3389/fphys.2015.00313 · Cited by 35 · see citing works
Sex differences in depression-like behavior after nerve injury are associated with differential changes in brain-derived neurotrophic factor levels in mice subjected to early life stress
Nishinaka, T., Kinoshita, M., Nakamoto, K., & Tokuyama, S. (2015) · Neuroscience Letters · doi:10.1016/j.neulet.2015.02.053 · Cited by 34 · see citing works
Sex-dependent effects of maternal separation on plasma corticosterone and brain monoamines in response to chronic ethanol administration
Kawakami, S. E., Quadros, I. M., Machado, R. B., & Suchecki, D. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.08.031 · Cited by 34 · see citing works
The Directive 2010/63/EU on animal experimentation may skew the conclusions of pharmacological and behavioural studies
Macrı̀, S., Ceci, C., Altabella, L., Canese, R., & Giovanni Laviola, A. (2013) · Scientific Reports · doi:10.1038/srep02380 · Cited by 31 · see citing works
Maternal separation modifies behavioural and neuroendocrine responses to stress in CCR7 deficient mice
Harrison, E. L., Jaehne, E. J., Jawahar, M. C., Corrigan, F., & Baune, B. T. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.01.036 · Cited by 29 · see citing works
Litter size is negatively correlated with corticosterone levels in weanling and juvenile laboratory rats
Rödel, H. G., Meyer, S., Prager, G., Stefanski, V., & Hudson, R. (2010) · Physiology & Behavior · doi:10.1016/j.physbeh.2010.01.032 · Cited by 29 · see citing works
Non-Human Primate Models of Alcohol-Related Phenotypes: The Influence of Genetic and Environmental Factors
Barr, C. S. (2011) · Current topics in behavioral neurosciences · doi:10.1007/7854_2011_142 · Cited by 27 · see citing works
Adrenocortical Mediation of the Effects of Early Life Experiences
Ader, R., & Grota, L. J. (1973) · Progress in brain research · doi:10.1016/s0079-6123(08)64095-9 · Cited by 27 · see citing works
Vulnerability of synaptic plasticity in the complexin II knockout mouse to maternal deprivation stress
Yamauchi, Y., Qin, L.-H., Nishihara, M., Sawada, K., Katō, K., & Inoue, S. (2005) · Brain Research · doi:10.1016/j.brainres.2005.07.015 · Cited by 27 · see citing works
Effects of Litter Size on Emotionality, Adrenocortical Reactivity, and Susceptibility to Gastric Erosions in the Rat
Grota, L. J., & Ader, R. (1969) · Psychological Reports · doi:10.2466/pr0.1969.24.2.547 · Cited by 24 · see citing works
Post-natal stress-induced endocrine and metabolic alterations in mice at adulthood involve different pro-opiomelanocortin-derived peptides
Loizzo, S., Campana, G., Vella, S., Fortuna, A., Galietta, G., Guarino, I., Costa, L., Capasso, A., Renzi, P., Frajese, G. V., et al. (2010) · Peptides · doi:10.1016/j.peptides.2010.08.001 · Cited by 24 · see citing works
Family matters: Maternal and litter-size effects on immune parameters in young laboratory rats
Prager, G., Stefanski, V., Hudson, R., & Rödel, H. G. (2010) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2010.07.240 · Cited by 23 · see citing works
Non-Human Primate Models of Alcohol-Related Phenotypes: The Influence of Genetic and Environmental Factors
Barr, C. S. (2011) · Current topics in behavioral neurosciences · doi:10.1007/978-3-642-28720-6_142 · Cited by 18 · see citing works
Effects of an Early Handling-Like Procedure and Individual Housing on Anxiety-Like Behavior in Adult C57BL/6J and DBA/2J Mice
Flanigan, T. J., & Cook, M. N. (2011) · PLoS ONE · doi:10.1371/journal.pone.0019058 · Cited by 14 · see citing works
Effects of maternal deprivation on later behavior in two inbred strains of mice
Newell, T. G. (1967) · Psychonomic Science · doi:10.3758/bf03330788 · Cited by 13 · see citing works
Partial maternal separation and adult emotionality in BALB/c mice
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Maternal separation alters social odor preference development in infant mice (Mus musculus).
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Severe maternal separation and adult emotional reactivity in BALB/c mice
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Maternal Separation and Emotional Reactivity in Balb/C Mice
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Animal models of major depression: drawbacks and challenges
Planchez, B., Surget, A., & Belzung, C. (2019) · Journal of Neural Transmission · doi:10.1007/s00702-019-02084-y · Cited by 480 · see citing works
Neurobiology of Resilience: Interface Between Mind and Body
Cathomas, F., Murrough, J. W., Nestler, E. J., Han, M.-H., & Russo, S. J. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.04.011 · Cited by 296 · see citing works
“If pups experience maternal-deprivation for a long period, they show higher susceptibility to subsequent stressors in adult life, HPA axis hyperactivity and altered glucocorticoid responses (34) (35).”
Background
Neural mechanisms of social homeostasis
Matthews, G. A., & Tye, K. M. (2019) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.14016 · Cited by 273 · see citing works
The future of rodent models in depression research
Gururajan, A., Reif, A., Cryan, J. F., & Slattery, D. A. (2019) · Nature Reviews Neuroscience · doi:10.1038/s41583-019-0221-6 · Cited by 269 · see citing works
The effects of early life stress on reward processing
Novick, A. M., Levandowski, M. L., Laumann, L. E., Philip, N. S., Price, L. H., & Tyrka, A. R. (2018) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2018.02.002 · Cited by 192 · see citing works
“One difficulty in characterizing the maternal separation literature is the wide variety of separation methods, control groups, and statistical methods that have been utilized (Lehmann and Feldon, 2000; Tractenberg et al., 2016).”
Method
The stressed brain of humans and rodents
Joëls, M., Karst, H., & Sarabdjitsingh, R. A. (2018) · Acta Physiologica · doi:10.1111/apha.13066 · Cited by 189 · see citing works
Animal Models of Depression: What Can They Teach Us about the Human Disease?
Becker, M., Pinhasov, A., & Ornoy, A. (2021) · Diagnostics · doi:10.3390/diagnostics11010123 · Cited by 185 · see citing works
Early life adversity shapes neural circuit function during sensitive postnatal developmental periods
Malave, L., van Dijk, M. T., & Anacker, C. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-02092-9 · Cited by 177 · see citing works
Early-life stress impairs postnatal oligodendrogenesis and adult emotional behaviour through activity-dependent mechanisms
Teissier, A., Magueresse, C. L., Olusakin, J., da Costa, B. L. S. A., Stasi, A. M. D., Bacci, A., Kawasawa, Y. I., Vaidya, V. A., & Gaspar, P. (2019) · Molecular Psychiatry · doi:10.1038/s41380-019-0493-2 · Cited by 154 · see citing works
Rodent tests of depression and anxiety: Construct validity and translational relevance
Gencturk, S., & Unal, G. (2024) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/s13415-024-01171-2 · Cited by 138 · see citing works
Systematic review and meta-analysis: effects of maternal separation on anxiety-like behavior in rodents
Wang, D., Levine, J. L. S., Avila-Quintero, V. J., Bloch, M. H., & Kaffman, A. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-0856-0 · Cited by 142 · see citing works
How Early Life Stress Impact Maternal Care: A Systematic Review of Rodent Studies
Orso, R., Creutzberg, K. C., Wearick‐Silva, L. E., Viola, T. W., Tractenberg, S. G., Benetti, F., & Grassi‐Oliveira, R. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00197 · Cited by 121 · see citing works
Animal models for bipolar disorder: from bedside to the cage
Beyer, D. K. E., & Freund, N. (2017) · International Journal of Bipolar Disorders · doi:10.1186/s40345-017-0104-6 · Cited by 110 · see citing works
Effects of Early-Life Stress on Social and Anxiety-Like Behaviors in Adult Mice: Sex-Specific Effects
Bondar, N. P., Lepeshko, A. A., & Reshetnikov, V. V. (2018) · Behavioural Neurology · doi:10.1155/2018/1538931 · Cited by 105 · see citing works
Limiting habenular hyperactivity ameliorates maternal separation-driven depressive-like symptoms
Tchenio, A., Lecca, S., Valentinova, K., & Mameli, M. (2017) · Nature Communications · doi:10.1038/s41467-017-01192-1 · Cited by 103 · see citing works
Early-life adversity and long-term neurobehavioral outcomes: epigenome as a bridge?
Vaiserman, A. M., & Koliada, A. K. (2017) · Human Genomics · doi:10.1186/s40246-017-0129-z · Cited by 96 · see citing works
Impact of juvenile chronic stress on adult cortico-accumbal function: Implications for cognition and addiction
Watt, M. J., Weber, M. A., Davies, S. R., & Forster, G. L. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.06.015 · Cited by 94 · see citing works
Altered corticolimbic connectivity reveals sex-specific adolescent outcomes in a rat model of early life adversity
Honeycutt, J. A., Demaestri, C., Peterzell, S., Silveri, M. M., Cai, X., Kulkarni, P. P., Cunningham, M. G., Ferris, C. F., & Brenhouse, H. C. (2020) · eLife · doi:10.7554/elife.52651 · Cited by 93 · see citing works
Vulnerability of the Hippocampus to Insults: Links to Blood–Brain Barrier Dysfunction
Davidson, T. L., & Stevenson, R. J. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25041991 · Cited by 77 · see citing works
The moderating effects of sex on consequences of childhood maltreatment: from clinical studies to animal models
White, J. D., & Kaffman, A. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.01082 · Cited by 73 · see citing works
Optogenetic and chemogenetic insights into the neurocircuitry of depression‐like behaviour: A systematic review
Biselli, T., Lange, S. S., Sablottny, L., Steffen, J., & Walther, A. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14603 · Cited by 72 · see citing works
Maternal separation effects on mother rodents’ behaviour: A systematic review
Alves, R. L., Portugal, C. C., Summavielle, T., Barbosa, F., & Magalhães, A. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.09.008 · Cited by 68 · see citing works
Encore: Behavioural animal models of stress, depression and mood disorders
Petković, A., & Chaudhury, D. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.931964 · Cited by 70 · see citing works
Lactobacillus paracasei PS23 reduced early-life stress abnormalities in maternal separation mouse model
Liao, J. F., Hsu, C.-P., Chou, G.-T., Hsu, J. S., Liong, M., & Tsai, Y.-C. (2019) · Beneficial Microbes · doi:10.3920/bm2018.0077 · Cited by 67 · see citing works
Translational studies identify long-term impact of prior neonatal pain experience
Walker, S. M. (2017) · Pain · doi:10.1097/j.pain.0000000000000784 · Cited by 66 · see citing works
Resilience priming: Translational models for understanding resiliency and adaptation to early life adversity
Kentner, A. C., Cryan, J. F., & Brummelte, S. (2019) · Developmental Psychobiology · doi:10.1002/dev.21775 · Cited by 64 · see citing works
The evolving neurobiology of early-life stress
Birnie, M. T., & Baram, T. Z. (2025) · Neuron · doi:10.1016/j.neuron.2025.02.016 · Cited by 65 · see citing works
Neuroimmune Impacts of Early-Life Stress on Development and Psychopathology
Brenhouse, H. C., Danese, A., & Grassi‐Oliveira, R. (2018) · Current topics in behavioral neurosciences · doi:10.1007/7854_2018_53 · Cited by 60 · see citing works
A Systematic Look at Environmental Modulation and Its Impact in Brain Development
Sale, A. (2017) · Trends in Neurosciences · doi:10.1016/j.tins.2017.10.004 · Cited by 62 · see citing works
Neurodevelopmental origins of substance use disorders: Evidence from animal models of early‐life adversity and addiction
Levis, S. C., Baram, T. Z., & Mahler, S. V. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15223 · Cited by 58 · see citing works
SiNiSan Ameliorates the Depression-Like Behavior of Rats That Experienced Maternal Separation Through 5-HT1A Receptor/CREB/BDNF Pathway
Cao, K., Shen, C., Yuan, Y., Bai, S., Yang, L., Guo, L., Zhang, R., & Shi, Y. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00160 · Cited by 57 · see citing works
Deficits in hippocampal-dependent memory across different rodent models of early life stress: systematic review and meta-analysis
Rocha, M., Wang, D., Avila-Quintero, V. J., Bloch, M. H., & Kaffman, A. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01352-4 · Cited by 56 · see citing works
The Effects of Early Life Stress on the Brain and Behaviour: Insights From Zebrafish Models
Eachus, H., Choi, M., & Ryu, S. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.657591 · Cited by 52 · see citing works
Effect of a multi-strain probiotic mixture consumption on anxiety and depression symptoms induced in adult mice by postnatal maternal separation
Santa, F. D., Strimpakos, G., Marchetti, N., Gargari, G., Torcinaro, A., Arioli, S., Mora, D., Petrella, C., & Vecchioli, S. F. (2024) · Microbiome · doi:10.1186/s40168-024-01752-w · Cited by 58 · see citing works
Maternal separation increases alcohol-drinking behaviour and reduces endocannabinoid levels in the mouse striatum and prefrontal cortex
Portero-Tresserra, M., Gracia-Rubio, I., Cantacorps, L., Pozo, O. J., Gómez-Gómez, A., Pastor, A., López-Arnau, R., de la Torre, R., & Valverde, O. (2018) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2018.02.003 · Cited by 55 · see citing works
The maternal-placental-fetal interface: Adaptations of the HPA axis and immune mediators following maternal stress and prenatal alcohol exposure
Ruffaner‐Hanson, C. D., Noor, S., Sun, M. S., Solomon, E. R., Marquez, L. E., Rodriguez, D. E., Allan, A. M., Caldwell, K. K., Bakhireva, L. N., & Milligan, E. D. (2022) · Experimental Neurology · doi:10.1016/j.expneurol.2022.114121 · Cited by 52 · see citing works
Adverse Behavioral Changes in Adult Mice Following Neonatal Repeated Exposure to Pain and Sucrose
Ranger, M., Tremblay, S., Chau, C. M. Y., Holsti, L., GRUNAU, R. E., & Goldowitz, D. (2019) · Frontiers in Psychology · doi:10.3389/fpsyg.2018.02394 · Cited by 54 · see citing works
Maternal separation affects expression of stress response genes and increases vulnerability to ethanol consumption
Magalhães, T. D. A., Correia, D., de Carvalho, L. M., Damasceno, S., & Godard, A. L. B. (2017) · Brain and Behavior · doi:10.1002/brb3.841 · Cited by 53 · see citing works
The effects of early life adversity on growth, maturation, and steroid hormones in male and female rats
Eck, S. R., Ardekani, C. S., Salvatore, M., Luz, S., Kim, E. D., Rogers, C. M., Hall, A., Lee, D. E., Famularo, S. T., Bhatnagar, S., et al. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14609 · Cited by 52 · see citing works
The paradox of care in behavioral epigenetics: Constructing early-life adversity in the lab
Lappé, M. D. (2018) · BioSocieties · doi:10.1057/s41292-017-0090-z · Cited by 51 · see citing works
Neurobiological Links between Stress, Brain Injury, and Disease
Guo, H., Zheng, L., Xu, H., Pang, Q., Ren, Z., Gao, Y. Z., & Wang, T. (2022) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2022/8111022 · Cited by 53 · see citing works
Early life stress and the programming of eating behavior and anxiety: Sex-specific relationships with serotonergic activity and hypothalamic neuropeptides
de Lima, R. M. S., Bento, L. V. D. S., Lugon, M. D. M. V., Baraúna, V. G., Bittencourt, A. S., Dalmaz, C., & Bittencourt, A. P. S. D. V. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.112399 · Cited by 50 · see citing works
Maternal behavior of the mouse dam toward pups: implications for maternal separation model of early life stress
Orso, R., Wearick‐Silva, L. E., Creutzberg, K. C., Centeno‐Silva, A., Roithmann, L. G., Pazzin, R., Tractenberg, S. G., Benetti, F., & Grassi‐Oliveira, R. (2017) · Stress · doi:10.1080/10253890.2017.1389883 · Cited by 49 · see citing works
Effect of early life stress on anxiety and depressive behaviors in adolescent mice
Ting, H., Guo, C., Wang, C., Hu, C., & Chen, H. (2020) · Brain and Behavior · doi:10.1002/brb3.1526 · Cited by 47 · see citing works
Resveratrol ameliorates maternal separation-induced anxiety- and depression-like behaviors and reduces Sirt1-NF-kB signaling-mediated neuroinflammation
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Maternal deprivation impairs memory and cognitive flexibility, effect that is avoided by environmental enrichment
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“The wrong tools for the right job”: a critical meta-analysis of traditional tests to assess behavioural impacts of early life stressPreprint
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Maternal Separation Does Not Produce a Significant Behavioral Change in Mice
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Authors: Tractenberg, S. G., Levandowski, M. L., de Azeredo, L. A., Orso, R., Roithmann, L. G., Hoffmann, E. S., Brenhouse, H., & Grassi-Oliveira, R.
Affiliations: Pontifícia Universidade Católica do Rio Grande do Sul (BR)
Northeastern University (US)
ORCID: Tractenberg, Saulo G.
Levandowski, Mateus L.
Orso, Rodrigo
Roithmann, Laura G.
Brenhouse, Heather
Venue: Neuroscience & Biobehavioral Reviews
Publisher: Elsevier BV
Published: 2016-09
Volume: 68
Pages: 489-503
ISSN: 0149-7634 (ISSN-L)
DOI: 10.1016/j.neubiorev.2016.06.021
OpenAlex: W2428176893
Cited by: 267
References: 138
Citations by year: 2026: 9 · 2025: 22 · 2024: 31 · 2023: 30 · 2022: 33 · 2021: 32 · 2020: 42 · 2019: 26 · 2018: 20 · 2017: 20 · 2016: 2
FWCI: 2.33
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neuroscience & Biobehavioral Reviews (publishedVersion)
PubMed (publishedVersion)
Funders: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
Conselho Nacional de Desenvolvimento Científico e Tecnológico
Topics: Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Social Sciences › Psychology › Clinical Psychology › Child Abuse and Trauma
Keywords: maternal separation, early life stress, behavioural outcomes, mice, methodological heterogeneity, reporting quality, stress exposure, developmental programming
MeSH terms: Animals, Animals, Newborn, Behavior, Animal, Maternal Deprivation, Stress, Psychological, Reproducibility of Results, Mice

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An overview of maternal separation effects on behavioural outcomes in mice: evidence from a four-stage methodological systematic review

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